Gap junctions in developing neocortex: A review

Brain Research Reviews

Volumn 47, Issue 1-3, 2004, Pages 216-226

  Montoro, Rafael J ^a,b   Yuste, Rafael ^a  

^a Och Spine at New York Presbyterian Hospitals   (United States)

^b UNIVERSITY OF SEVILLE   (Spain)

Author keywords

Development; Development and regeneration; Formation and specificity of synapses; Gap junction; Neocortex

Indexed keywords

GAP JUNCTION PROTEIN;

BRAIN DEVELOPMENT; CELL ACTIVATION; CELL COMMUNICATION; CELL DIFFERENTIATION; CELL FUNCTION; CONFERENCE PAPER; ELECTROPHYSIOLOGY; GAP JUNCTION; HUMAN; IMAGING SYSTEM; NEOCORTEX; NERVE CELL; NERVE CELL NETWORK; NERVOUS SYSTEM DEVELOPMENT; NEUROBLAST; NEUROIMAGING; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; CELL COMMUNICATION; CELL DIFFERENTIATION; CONNEXINS; GAP JUNCTIONS; HUMANS; NEOCORTEX; NEURAL PATHWAYS; NEURONS; STEM CELLS;

EID: 9644289646     PISSN: 01650173     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainresrev.2004.06.009     Document Type: Conference Paper

References (105)

1. Anzini P., Neuberg D.H., Schachner M., Nelles E., Willecke K., Zielasek J., Toyka K.V., Suter U., Martini R. Structural abnormalities and deficient maintenance of peripheral nerve myelin in mice lacking the gap junction protein connexin 32. J. Neurosci. 17:1997;4545-4551
2. Baker R., Llinas R. Electrotonic coupling between neurones in the rat mesencephalic nucleus. J. Physiol. 212:1971;45-63
3. Bahrey H.L., Moody W.J. Voltage-gated currents, dye and electrical coupling in the embryonic mouse neocortex. Cereb. Cortex. 13:2003;239-251
4. Belluardo N., Mud G., Trovato-Salinaro A., Le Gurun S., Charollais A., Serre-Beinier V., Amato G., Haefliger J.A., Meda P., Condorelli D.F. Expression of connexin36 in the adult and developing rat brain. Brain Res. 865:2000;121-138
5. Bennett M.V.L. Electrical synapses, a personal perspective (or history). Brain Res. Rev. 32:2000;16-28
6. Bennett M.V.L., Aljure E., Nakajima Y., Pappas G.D. Electrotonic junctions between teleost spinal neurons: electrophysiology and ultrastructure. Science. 141:1963;262
7. Berger B., Verney C., Alvarez C., Vigny A., Helle K.B. New dopaminergic terminal fields in the motor, visual (area 18b) and retrosplenial cortex in the young and adult rat. Immunocytochemical and catecholamine histochemical analyses. Neuroscience. 15:1985;983-998
8. Bergoffen J., Scherer S.S., Wang S., Scott M.O., Bone L.J., Paul D.L., Chen K., Lensch M.W., Chance P.F., Fischbeck K.H. Connexin mutations in X-linked Charcot-Marie-Tooth disease. Science. 262:1993;2039-2042
9. Bittman K.S., LoTurco J.J. Differential regulation of connexin 26 and 43 in murine neocortical precursors. Cereb. Cortex. 9:1999;188-195
10. Bittman K., Owens D.F., Kriegstein A.R., LoTurco J.J. Cell coupling and uncoupling in the ventricular zone of developing neocortex. J. Neurosci. 17:1997;7037-7044
11. Bittman K., Becker D.L., Cicirata F., Parnavelas J.G. Connexin expression in homotypic and heterotypic cell coupling in the developing cerebral cortex. J. Comp. Neurol. 443:2002;201-212
12. Blue M.E., Parnavelas J.G. The formation and maturation of synapses in the visual cortex of the rat: II. Quantitative analysis. J. Neurocytol. 12:1983;697-712
13. Bohn L.M., Xu F., Gainetdinov R.R., Caron M.G. Potentiated opioid analgesia in norepinephrine transporter knock-out mice. J. Neurosci. 20:2000;9040-9045
14. Chang Q., Balice-Gordon R.J. Gap junctional communication among developing and injured motor neurons. Brain Res. Rev. 32:2000;242-249
15. Condorelli D.F., Trovato-Salinaro A., Mudo G., Mirone M.B., Belluardo N. Cellular expression of connexins in the rat brain: neuronal localization, effects of kainate-induced seizures and expression in apoptotic neuronal cells. Eur. J. Neurosci. 18:2003;1807-1827
16. Connors B.W., Benardo L.S., Prince D.A. Coupling between neurons of the developing rat neocortex. J. Neurosci. 3:1983;773-782
17. Cotrina M.L., Lin J.H., Alves-Rodrigues A., Liu S., Li J., Azmi-Ghadimi H., Kang J., Naus C.C., Nedergaard M. Connexins regulate calcium signaling by controlling ATP release. Proc. Natl. Acad. Sci. U. S. A. 95:1998;15735-15740
18. D'Amato R.J., Blue M.E., Largent B.L., Lynch D.R., Ledbetter D.J., Molliver M.E., Snyder S.H. Ontogeny of the serotonergic projection to rat neocortex: transient expression of a dense innervation to primary sensory areas. Proc. Natl. Acad. Sci. U. S. A. 84:1987;4322-4326
19. Deans M.R., Gibson J.R., Sellitto C., Connors B.W., Paul D.L. Synchronous activity of inhibitory networks in neocortex requires electrical synapses containing connexin36. Neuron. 31:2001;477-485
20. Dermietzel R., Traub O., Hwang T.K., Beyer E., Bennett M.V.L., Spray D.C., Willecke K. Differential expression of three gap junction proteins in developing and mature brain tissues. Proc. Natl. Acad. Sci. U. S. A. 86:1989;10148-10152
21. Dermietzel R., Farooq M., Kessler J.A., Althaus H., Hertzberg E.L., Spray D.C. Oligodendrocytes express gap junction proteins connexin32 and connexin45. Glia. 20:1997;101-114
22. Devor A., Yarom Y. Electrotonic coupling in the inferior olivary nucleus revealed by simultaneous double patch recordings. J. Neurophysiol. 87:2002;3048-3058
23. Fatt P., Katz B. An analysis of the end-plate potential recorded with an intracellular electrode. J. Physiol. 115:1951;320-370
24. Furshpan E.J., Potter D.D. Transmission at the giant motor synapses of the crayfish. J. Physiol. 145:1959;289-325
25. Fushiki S., Perez Velazquez J.L., Zhang L., Bechberger J.F., Carlen P.L., Naus C.C. Changes in neuronal migration in neocortex of connexin43 null mutant mice. J. Neuropathol. Exp. Neurol. 62:2003;304-314
26. Gabriel H.D., Jung D., Butzler C., Temme A., Traub O., Winterhager E., Willecke K. Transplacental uptake of glucose is decreased in embryonic lethal connexin26-deficient mice. J. Cell Biol. 140:1998;1453-1461
27. Galarreta M., Hestrin S. Electrical synapses between GABA-releasing interneurons. Nat. Rev., Neurosci. 2:2001;425-433
28. Garaschuk O., Linn J., Eilers J., Konnerth A. Large-scale oscillatory calcium waves in the immature cortex. Nat. Neurosci. 3:2000;452-459
29. Giaume C., Fromaget C., el Aoumari A., Cordier J., Glowinski J., Gros D. Gap junctions in cultured astrocytes: single-channel currents and characterization of channel-forming protein. Neuron. 6:1991;133-143
30. Gibson J.R., Beierlein M., Connors B.W. Two networks of electrically coupled inhibitory neurons in neocortex. Nature. 402:1999;75-79
31. Goodenough D.A., Goliger J.A., Paul D.L. Connexins, connexons, and intercellular communication. Annu. Rev. Biochem. 65:1996;475-502
32. Guthrie S.C., Gilula N.B. Gap junctional communication and development. TINS. 12:1989;12-16
33. Gutnick M.J., Prince D.A. Dye coupling and possible electrotonic coupling in the guinea pig neocortical slice. Science. 211:1981;67-70
34. Hauswirth O. The influence of halothane on the electrical properties of cardiac Purkinje fibres. J. Physiol. 210:1969;42-43
35. Hille B. Ion Channels of Excitable Membranes. 3rd ed.:2001;Sinauer Associates, Sunderland
36. Hormuzdi S.G., Pais I., LeBeau F.E., Towers S.K., Rozov A., Buhl E.L., Whittington M.A., Monyer H. Impaired electrical signaling disrupts gamma frequency oscillations in connexin 36-deficient mice. Neuron. 31:2001;487-495
37. Hubel D.H., Wiesel T.N. Functional architecture of the macaque monkey visual cortex. Proc. R. Soc. Lond., B Biol. sci. 198:1977;1-59
38. Kandler K., Katz L.C. Neuronal coupling and uncoupling in the developing nervous system. Curr. Opin. Neurobiol. 5:1995;98-105
39. Kandler K., Katz L.C. Coordination of neuronal activity in developing visual cortex by gap junction-mediated biochemical communication. J. Neurosci. 18:1998;1419-1427
40. Kandler K., Katz L.C. Relationship between dye coupling and spontaneous activity in developing ferret visual cortex. Dev. Neurosci. 20:1998;59-64
41. Katz L.C. Coordinate activity in retinal and cortical development. Curr. Opin. Neurobiol. 3:1993;93-99
42. Korn H., Sotelo C., Crepel F. Electronic coupling between neurons in the rat lateral vestibular nucleus. Exp. Brain Res. 16:1973;255-275
43. Kumar N.M., Gilula N.B. The gap junction communication channel. Cell. 84:1996;381-388
44. Kunzelmann P., Blumcke I., Traub O., Dermietzel R., Willecke K. Coexpression of connexin45 and 32 in oligodendrocytes of rat brain. J. Neurocytol. 26:1997;17-22
45. Leslie C.A., Robertson M.W., Cutler A.J., Bennett J.P. Jr. Postnatal development of D1 dopamine receptors in the medial prefrontal cortex, striatum and nucleus accumbens of normal and neonatal 6-hydroxydopamine treated rats: a quantitative autoradiographic analysis. Dev. Brain Res. 62:1991;109-114
46. Levitt P., Moore R.Y. Development of the noradrenergic innervation of neocortex. Brain Res. 162:1979;243-259
47. Levitt P., Rakic P. Immunoperoxidase localization of glial fibrillary acidic protein in radial glial cells and astrocytes of the developing rhesus monkey brain. J. Comp. Neurol. 193:1980;815-840
48. Lorente de Nó R. Cerebral Cortex: architecture, intracortical connections, motor projections. Fulton J.F. Physiology of the Nervous System. 1949;228-330 Oxford Univ. Press, New York
49. LoTurco J.J., Kriegstein A.R. Clusters of coupled neuroblasts in embryonic neocortex. Science. 252:1991;563-566
50. LoTurco J.J., Owens D.F., Heath M.J., Davis M.B., Kriegstein A.R. GABA and glutamate depolarize cortical progenitor cells and inhibit DNA synthesis. Neuron. 15:1995;1287-1298
51. MacVicar B.A., Dudek F.E. Electrotonic coupling between pyramidal cells: a direct demonstration in rat hippocampal slices. Science. 213:1981;782-785
52. Maxeiner S., Kruger O., Schilling K., Traub O., Urschel S., Willecke K. Spatiotemporal transcription of connexin45 during brain development results in neuronal expression in adult mice. Neuroscience. 119:2003;689-700
53. McDonald J.K., Petrovic S.L., McCann S.M., Parnavelas J.G. The development of beta-adrenergic receptors in the visual cortex of the rat. Neuroscience. 7:1982;2649-2655
54. Moreno A.P., Laing J.G., Beyer E.C., Spray D.C. Properties of gap junction channels formed of connexin 45 endogenously expressed in human hepatoma (SKHep1) cells. Am. J. Physiol. 268:1995;C356-C365
55. Meyer T. Cell signaling by second messenger waves. Cell. 64:1991;675-678
56. Meyer A.H., Katona I., Blatow M., Rozov A., Monyer H. In vivo labeling of parvalbumin-positive interneurons and analysis of electrical coupling in identified neurons. J. Neurosci. 22:2002;7055-7064
57. Mienville J.M., Lange G.D., Barker J.L. Reciprocal expression of cell-cell coupling and voltage-dependent Na current during embryogenesis of rat telencephalon. Dev. Brain Res. 77:1994;89-95
58. Mountcastle V.B. An organizing principle of cerebral function: the unit module and the distributed system. Schmitt H.O. The Mindful Brain. 1982;1-50 MIT Press, Cambridge, Massachussetts
59. Nadarajah B., Jones A.M., Evans W.H., Parnavelas J.G. Differential expression of connexins during neocortical development and neuronal circuit formation. J. Neurosci. 17:1997;3096-3111
60. Nadarajah B., Makarenkova H., Becker D.L., Evans W.H., Parnavelas J.G. Basic FGF increases communication between cells of the developing neocortex. J. Neurosci. 18:1998;7881-7890
61. Naus C.C., Bani-Yaghoub M. Gap junctional communication in the developing central nervous system. Cell Biol. Int. 22:1998;751-763
62. Newman E.A., Zahs K.R. Calcium waves in retinal glial cells. Science. 275:1997;844-847
63. Nishii K., Kumai M., Egashira K., Miwa T., Hashizume K., Miyano Y., Shibata Y. Mice lacking connexin45 conditionally in cardiac myocytes display embryonic lethality similar to that of germline knockout mice without endocardial cushion defect. Cell Adhes. Commun. 10:2003;365-369
64. Okada H., Miyakawa N., Mori H., Mishina M., Miyamoto Y., Hisatsune T. NMDA receptors in cortical development are essential for the generation of coordinated increases in [Ca2+](i) in "neuronal domains" Cereb. Cortex. 13:2003;749-757
65. Owens D.F., Kriegstein A.R. Patterns of intracellular calcium fluctuation in precursor cells of the neocortical ventricular zone. J. Neurosci. 18:1998;5374-5388
66. Owens D.F., Flint A.C., Dammerman R.S., Kriegstein A.R. Calcium dynamics of neocortical ventricular zone cells. Dev. Neurosci. 22:2000;25-33
67. Peinado A. Traveling slow waves of neural activity: a novel form of network activity in developing neocortex. J. Neurosci. 20:2000;RC54
68. Peinado A. Immature neocortical neurons exist as extensive syncytial networks linked by dendrodendritic electrical connections. J. Neurophysiol. 85:2001;620-629
69. Peinado A., Yuste R., Katz L.C. Extensive dye coupling between rat neocortical neurons during the period of circuit formation. Neuron. 10:1993;103-114
70. Peinado A., Yuste R., Katz L.C. Gap junctional communication and the development of local circuits in neocortex. Cereb. Cortex. 3:1993;488-498
71. Penn A., Wong R., Schatz C. Neuronal coupling in the developing mammalian retina. J. Neurosci. 14:1994;3805-3815
72. Perez Velazquez J.L., Frantseva M., Naus C.C., Bechberger J.F., Juneja S.C., Velumian A., Carlen P.L., Kidder G.M., Mills L.R. Development of astrocytes and neurons in cultured brain slices from mice lacking connexin43. Dev. Brain Res. 97:1996;293-296
73. Prime G., Horn G., Sutor B. Time-related changes in connexin mRNA abundance in the rat neocortex during postnatal development. Dev. Brain Res. 119:2000;111-125
74. Ralph R.J., Paulus M.P., Fumagalli F., Caron M.G., Geyer M.A. Prepulse inhibition deficits and perseverative motor patterns in dopamine transporter knock-out mice: differential effects of D1 and D2 receptor antagonists. J. Neurosci. 21:2001;305-313
75. Ramon y Cajal S. Histologie du Systeme Nerveux de l'Homme et des Vertebrates. 1911;Maloine, Paris
76. Rash J.E., Staines W.A., Yasumura T., Patel D., Furman C.S., Stelmack G.L., Nagy J.I. Immunogold evidence that neuronal gap junctions in adult rat brain and spinal cord contain connexin-36 but not connexin-32 or connexin-43. Proc. Natl. Acad. Sci. U. S. A. 97:2000;7573-7578
77. Reaume A.G., de Sousa P.A., Kulkarni S., Langille B.L., Zhu D., Davies T.C., Juneja S.C., Kidder G.M., Rossant J. Cardiac malformation in neonatal mice lacking connexin43. Science. 267:1995;1831-1834
78. Reuss B., Dermietzel R., Unsicker K. Fibroblast growth factor 2 (FGF-2) differentially regulates connexin (cx) 43 expression and function in astroglial cells from distinct brain regions. Glia. 22:1998;19-30
79. Roerig B., Feller M.B. Neurotransmitters and gap junctions in developing neural circuits. Brain Res. Rev. 32:2000;86-114
80. Roerig B., Sutor B. Regulation of gap junction coupling in the developing neocortex. Mol. Neurobiol. 12:1996;225-249
81. Roerig B., Sutor B. Serotonin regulates gap junction coupling in the developing rat somatosensory cortex. Eur. J. Neurosci. 8:1996;1685-1695
82. Roerig B., Sutor B. Nitric oxide-stimulated increase in intracellular cGMP modulates gap junction coupling in rat neocortex. NeuroReport. 7:1996;569-572
83. Roerig B., Klausa G., Sutor B. Beta-adrenoreceptor activation reduces dye-coupling between immature rat neocortical neurons. NeuroReport. 6:1995;1811-1815
84. Roerig B., Klausa G., Sutor B. Dye coupling between pyramidal neurons in developing rat prefrontal and frontal cortex is reduced by protein kinase A activation and dopamine. J. Neurosci. 15:1995;7386-7400
85. Roerig B., Klausa G., Sutor B. Intracellular acidification reduced gap junction coupling between immature rat neocortical pyramidal neurons. J. Physiol. 490:1996;31-49
86. Saez J.C., Berthoud V.M., Branes M.C., Martinez A.D., Beyer E.C. Plasma membrane channels formed by connexins: their regulation and functions. Physiol. Rev. 83:2003;1359-1400
87. Sherrington C.S. The Integrative Action of the Nervous System. 1906;C. Scribner's Sons, New York
88. Sloper J.J. Gap junctions between dendrites in the primate neocortex. Brain Res. 44:1972;641-646
89. Sohl G., Willecke K. An update on connexin genes and their nomenclature in mouse and man. Cell Adhes. Commun. 10:2003;173-180
90. Srinivas M., Rozental R., Kojima T., Dermietzel R., Mehler M., Condorelli D.F., Kessler J.A., Spray D.C. Functional properties of channels formed by the neuronal gap junction protein connexin36. J. Neurosci. 19:1999;9848-9855
91. Sutor B. Gap junctions and their implications for neurogenesis and maturation of synaptic circuitry in the developing neocortex. Results Probl. Cell Differ. 39:2002;53-73
92. Sutor B., Luhmann H.J. Development of excitatory and inhibitory postsynaptic potentials in the rat neocortex. Perspect. Dev. Neurobiol. 2:1995;409-419
93. Sutor B., Schmolke C., Teubner B., Schirmer C., Willecke K. Myelination defects and neuronal hyperexcitability in the neocortex of connexin 32-deficient mice. Cereb. Cortex. 10:2000;684-697
94. Theis M., Sohl G., Speidel D., Kuhn R., Willecke K. Connexin43 is not expressed in principal cells of mouse cortex and hippocampus. Eur. J. Neurosci. 18:2003;267-274
95. Traub R.D., Pais I., Bibbig A., LeBeau F.E., Buhl E.H., Hormuzdi S.G., Monyer H., Whittington M.A. Contrasting roles of axonal (pyramidal cell) and dendritic (interneuron) electrical coupling in the generation of neuronal network oscillations. Proc. Natl. Acad. Sci. U. S. A. 100:2003;1370-1374
96. Turin L., Warner A.E. Intracellular pH in early Xenopus embryos: its effect on current flow between blastomeres. J. Physiol. 300:1980;489-504
97. Vaney D.I. Many diverse types of retinal neurons show tracer coupling when injected with biocytin or Neurobiotin. Neurosci. Lett. 125:1991;187-190
98. Veenstra R.D., Wang H.Z., Beblo D.A., Chilton M.G., Harris A.L., Beyer E.C., Brink P.R. Selectivity of connexin-specific gap junctions does not correlate with channel conductance. Circ. Res. 77:1995;1156-1165
99. Venance L., Rozov A., Blatow M., Burnashev N., Feldmeyer D., Monyer H. Connexin expression in electrically coupled postnatal rat brain neurons. Proc. Natl. Acad. Sci. U. S. A. 97:2000;10260-10265
100. Watanabe A. The interaction of electrical activity among neurons of lobster cardiac ganglion. Jpn. J. Physiol. 8:1958;305-318
101. Wendlandt S., Crow T.J., Stirling R.V. The involvement of the noradrenergic system arising from the locus coeruleus in the postnatal development of the cortex in rat brain. Brain Res. 125:1977;1-9
102. Yuste R. Introduction: spontaneous activity in the developing central nervous system. Semin. Cell Dev. Biol. 8:1997;1-4
103. Yuste R., Katz L.C. Control of postsynaptic Ca2+ influx in developing neocortex by excitatory and inhibitory neurotransmitters. Neuron. 6:1991;333-344
104. Yuste R., Peinado A., Katz L.C. Neuronal domains in developing neocortex. Science. 257:1992;665-669
105. Yuste R., Nelson D.A., Rubin W.W., Katz L.C. Neuronal domains in developing neocortex: mechanisms of coactivation. Neuron. 14:1995;7-17